Russian J. Theriol. 12(1): 1932 © RUSSIAN JOURNAL OF THERIOLOGY, 2013 Analysis of shape and size variation of the first lower molar in Far-Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics Leonid L. Voyta*, Fedor N. Golenishchev & Mikhail P. Tiunov ABSTRACT. The variation of quantitative characters of the first lower molar was analysed in nine species of Far-Eastern voles Alexandromys from Russian fauna. Canonical variation analysis revealed that main differences were associated with oeconomus-like fusion, and clearly differentiates A. oeconomus, A. mongolicus and A. gromovi from other species. The results of UPGMA cluster analysis based on the average Procrustes distances did not agree with recent molecular studies. Discriminant analysis of Pro- crustes coordinates of 19 landmarks showed that the percentage of correct species classifications of samples vary from 50% to 100%. Linear measurements together with shape features can be used for identification of the following species: A. oeconomus, A. mongolicus, and A.sachalinensis. Shape of enamel loops of the first lower molar of Far-Eastern grey voles can be used for species identification, but not for phylogenetic analysis. KEY WORDS: Alexandromys, Far-Eastern grey voles, Rodentia, Russian fauna, relationships, species identification, first lower molar, geometric morphometrics. Leonid L. Voyta [[email protected]], Zoological Institute of the Russian Academy of Sciences. Univer- sitetskaya emb., 1, St.-Petersburg, 199034, Russia; Institute of Natural Resources, Ecology and Cryology of the Siberian Division of the Russian Academy of Sciences. Butina st., 26, Chita, 672090, Russia; Fedor N. Golenishchev [[email protected]], Zoological Institute of the Russian Academy of Sciences. Universitetskaya emb., 1, St.-Petersburg, 199034, Russia; & Mikhail P. Tiunov [[email protected]], Institute of Biology and Soil Science, Far East Division, Russian Academy of Sciences, Vladivostok 690022, Russia. Àíàëèç èçìåí÷èâîñòè ôîðìû è ðàçìåðîâ ïåðâîãî íèæíåãî êîðåííîãî çóáà äàëüíåâîñòî÷íûõ ñåðûõ ïîëåâîê ðîäà Alexandromys (Rodentia: Cricetidae) ôàóíû Ðîññèè ñ èñïîëüçîâàíèåì ãåîìåòðè÷åñêîé ìîðôîìåòðèè Ë.Ë. Âîéòà*, Ô.Í. Ãîëåíèùåâ, Ì.Ï. Òèóíîâ ÐÅÇÞÌÅ.  ðàáîòå ïðîàíàëèçèðîâàíà èçìåí÷èâîñòü êîëè÷åñòâåííûõ ïðèçíàêîâ ïåðâîãî íèæíåãî êîðåííîãî çóáà äåâÿòè âèäîâ äàëüíåâîñòî÷íûõ ïîëåâîê ðîäà Alexandromys (Rodentia: Cricetidae) ôàóíû Ðîññèè. Êàíîíè÷åñêèé âàðèàöèîííûé àíàëèç âûÿâèë, ÷òî îñíîâíûå ðàçëè÷èÿ ñâÿçàíû ñ «ýêîíîìóñíûì» ñëèÿíèåì, êîòîðîå õîðîøî äèôôåðåíöèðóåò A. oeconomus, A. mongolicus è A. gromovi îò äðóãèõ âèäîâ. Ðåçóëüòàò êëàñòåðíîãî àíàëèçà (ìåòîä UPGMA) îñíîâàííîãî íà ñðåäíèõ çíà÷åíèÿõ ïðîêðóñòîâûõ äèñòàíöèé íå ñîãëàñóåòñÿ ñ ðåçóëüòàòàìè ñîâðåìåííûõ ìîëåêóëÿðíûõ èññëåäîâàíèé. Äèñêðèìèíàíòíûé àíàëèç ïî ïðîêðóñòîâûì êîîðäèíàòàì 19 ìåòîê ïîêàçàë òî÷íîñòü êîððåêòíîé êëàññèôèêàöèè äëÿ âñåõ ïàð âèäîâ îò 50% äî 100%. Ëèíåéíûå ïðîìåðû â ñîâîêóïíîñòè ñ ïàðàìåòðàìè ôîðìû ìîãóò áûòü èñïîëüçîâàíû äëÿ îïðåäåëåíèÿ ñëåäóþùèõ âèäîâ: A. oeconomus, A. mongolicus, A. sachalinensis. Ôîðìà ýìàëåâûõ ïåòåëü ïåðâîãî íèæíåãî êîðåííîãî çóáà äàëüíåâî- ñòî÷íûõ ñåðûõ ïîëåâîê ìîæåò áûòü èñïîëüçîâàíà äëÿ îïðåäåëåíèé âèäà, íî íå äëÿ âûÿñíåíèÿ ðîäñòâåííûõ âçàèìîîòíîøåíèé â ãðóïïå. ÊËÞ×ÅÂÛÅ ÑËÎÂÀ: Alexandromys, äàëüíåâîñòî÷íûå ñåðûå ïîëåâêè, Rodentia, ôàóíà Ðîññèè, ôèëîãåíåòè÷åñêèå îòíîøåíèÿ, îïðåäåëåíèå âèäîâ, ïåðâûé íèæíèé êîðåííîé çóá, ãåîìåòðè÷åñêàÿ ìîðôîìåòðèÿ. * Corresponding author 20 L.L. Voyta, F.N. Golenishchev, M.P. Tiunov Introduction During the last decade the species number and taxo- nomic relationships of the Far-Eastern voles were de- Investigations of taxonomic status and relationships fined more exactly (Frisman et al., 2009; Sheremetyeva of the Far-Eastern grey voles from East Siberia and et al., 2009, Bannikova et al., 2010; Lissovsky et al., Russian Far East have a long history. This issue was 2010; Haring et al., 2011; Lissovsky & Obolenskaya, reviewed several times (Poljakov, 1881; Vinogradov, 2011; Abramson & Lissovsky, 2012). The inclusion of 1933; Ognev, 1950; Vinogradov & Gromov, 1952; A. mongolicus and A. middendorffii into Alexandromys Gromov et al., 1963; Kuziakin, 1963; Gromov & Poly- subgenus was supported with mitochondrial and mor- akov, 1977; Zagorodnyuk, 1990; Pozdniakov, 1993; phological data (Bannikova et al., 2010; Lissovsky et Meyer et al., 1996; Litvinov, 2001; Kartavtseva et al., al., 2010; Haring et al., 2011; Lissovsky & Obolen- skaya, 2011). One taxon of subspecific rank A. m. 2008; Frisman et al., 2009; Sheremetyeva et al., 2009; gromovi was elevated to the species status A. gro- Bannikova et al., 2010; Lissovsky et al., 2010; Liss- movi (Sheremetyeva et al., 2009), which is closely ovsky & Obolenskaya, 2010, 2011; Haring et al., 2011; phylogenetically related to A. middendorffii and A. mon- Abramson & Lissovsky, 2012). golicus (Bannikova et al., 2010; Lissovsky et al., 2010). At present the Far-Eastern voles are assigned to the According to this information, nine species inhabit Rus- genus Alexandromys Ognev, 1914 (Abramson & Liss- sian part of Alexandromys distribution: A. fortis, A. ovsky, 2012). We accept this opinion and will use maximowiczii, A. sachalinensis, A. mujanensis, A. evo- Alexandromys instead Microtus below. ronensis, A. middendorffii, A. mongolicus, A. gromovi During the last threefour decades the discussion on and A. oeconomus Pallas, 1776 (Abramson & Liss- taxonomy of Far-Eastern voles was focused on two ovsky, 2012). main questions: (a) taxonomic relationships between Despite of some progress in the phylogeny and species, and (b) species identification. taxonomic composition of the genus, the problem of Karyological studies of the second half of the 20th species identification is still pressing. It is especially century revealed high chromosomal variation in A. max- true for fossil remains which are commonly identifiable imowiczii Schrenk, 1858 (Kovalskaja et al., 1980; Kar- on the basis of occlusal molar pattern only (Rabeder, tavtseva et al., 2008), and three new cryptic taxa were 1981; Agadzhanian & Yatsenko, 1984; Kazantseva & described: A. mujanensis Orlov et Kovalskaja, 1975, A. Tesakov, 1998; Martin, 1998; Tesakov, 2005). The evoronensis Kovalskaja et Sokolov, 1980, A. maxi- identifying of fossil material demands special care in mowiczii gromovi Vorontsov et al., 1988. Re-examina- using modern morphometric techniques applied to the tion of Alexandromys species using karyological tech- grey voles dentition. Thereby, the main tasks of the niques (including hybridological studies) supported the present study is to analyse an interspecific variation of validity of five species in the subgenus, which were the first lower molar (m1) of Far-Eastern grey voles included previously in different species groups (Meyer from Russian fauna and to evaluate the identification et al., 1996) or even subgenera (Gromov & Erbaeva, power of the dental quantitative features in this group 1995). These species were: A. fortis Büchner, 1889, A. of voles. maximowiczii, A. sachalinensis Vasin, 1955, A. mujan- ensis and A. evoronensis. In spite of the published Material and methods identification keys and detailed morphological descrip- tion (Gromov & Polyakov, 1977; Golenishchev, 1982) these five species were difficult to identify morpholog- We studied collections of Zoological Institute of the ically (Pozdniakov, 1993; Voyta & Golenishchev, 2007, Russian Academy of Sciences (ZIN; St.-Petersburg, 2008; Voyta et al., 2011). The similarity in the shape of Russia), Zoological Museum of Moscow State Univer- enamel loops of molars between different species (Rörig sity (ZMMU; Moscow, Russia), Institute of Plant and & Börner, 1905; Hinton, 1929; Zimmermann, 1952, Animal Ecology of the Russian Academy of Sciences 1959; Angermann, 1973; Gromov & Polyakov, 1977; (IPAE; Yekaterinburg, Russia), Institute of Biology Koenigswald, 1980; Butler, 1985) causes a consider- and Soil Science of the Far East division of the Russian able problem for diagnostics, particularly dealing with Academy of Sciences (IBSS; Vladivostok, Russia), as fossil remains (Rabeder, 1981; Kotlia & Mathur, 1992). well as two private collections: Marina N. Meyers In this case, the geographical distribution becomes an Private Collection (MM), stored in Zoological Institute important criterion for species identification (Shenbrot and field collection (FN IBSS), stored in Institute of & Krasnov, 2005), since three species (A. sachalinen- Biology and Soil Science (Appendix 1). The museum sis, A. mujanensis and A. evoronensis) have a restricted specimens, mentioned in the text, were labelled with distribution, while two others were found to have over- museum abbreviation followed with collection ID, for lapping ranges but differ in ecological preferences (Gro- example: IBSS-10944. mov & Erbaeva, 1995; Meyer et al., 1996). Some In total, 433 left m1 of nine species mentioned studies discussed including of Microtus mongolicus above were analysed. This sample includes animals Radde, 1861 (Meyer et al., 1996) and M. middendorffii from captivity as well as wild animals. Poljakov, 1881 (Zagorodnyuk, 1990) into the subgenus Taking into account problems with species identifi- Alexandromys also. cation (Voyta & Golenishchev, 2008; Voyta et al., Analysis of molar variation of Far-Eastern voles 21 Figure 1. Scheme of morphological terms, measurements and landmarks position. A the elements of the m1 occlusal pattern of grey voles: Asd the position of anterior dentine tract